Novel indices reveal that pollinator exposure to pesticides varies across biological compartments and crop surroundings.

Declines in insect pollinators have been linked to a range of causative factors such as disease, loss of habitats, the quality and availability of food, and exposure to pesticides. Here, we analysed an extensive dataset generated from pesticide screening of foraging insects, pollen-nectar stores/beebread, pollen and ingested nectar across three species of bees collected at 128 European sites set in two types of crop. In this paper, we aimed to (i) derive a new index to summarise key aspects of complex pesticide exposure data and (ii) understand the links between pesticide exposures depicted by the different matrices, bee species and apple orchards versus oilseed rape crops. We found that summary indices were highly correlated with the number of pesticides detected in the related matrix but not with which pesticides were present. Matrices collected from apple orchards generally contained a higher number of pesticides (7.6 pesticides per site) than matrices from sites collected from oilseed rape crops (3.5 pesticides), with fungicides being highly represented in apple crops. A greater number of pesticides were found in pollen-nectar stores/beebread and pollen matrices compared with nectar and bee body matrices. Our results show that for a complete assessment of pollinator pesticide exposure, it is necessary to consider several different exposure routes and multiple species of bees across different agricultural systems.

Fertilizer and herbicide alter nectar and pollen quality with consequences for pollinator floral choices.

Background: Pollinating insects provide economically and ecologically valuable services, but are threatened by a variety of anthropogenic changes. The availability and quality of floral resources may be affected by anthropogenic land use. For example, flower-visiting insects in agroecosystems rely on weeds on field edges for foraging resources, but these weeds are often exposed to agrochemicals that may compromise the quality of their floral resources. Methods: We conducted complementary field and greenhouse experiments to evaluate the: (1) effect of low concentrations of agrochemical exposure on nectar and pollen quality and (2) relationship between floral resource quality and insect visitation. We applied the same agrochemcial treatments (low concentrations of fertilizer, low concentrations of herbicide, a combination of both, and a control of just water) to seven plant species in the field and greenhouse. We collected data on floral visitation by insects in the field experiment for two field seasons and collected pollen and nectar from focal plants in the greenhouse to avoid interfering with insect visitation in the field. Results: We found pollen amino acid concentrations were lower in plants exposed to low concentrations of herbicide, and pollen fatty acid concentrations were lower in plants exposed to low concentrations of fertilizer, while nectar amino acids were higher in plants exposed to low concentrations of either fertilizer or herbicide. Exposure to low fertilizer concentrations also increased the quantity of pollen and nectar produced per flower. The responses of plants exposed to the experimental treatments in the greenhouse helped explain insect visitation in the field study. The insect visitation rate correlated with nectar amino acids, pollen amino acids, and pollen fatty acids. An interaction between pollen protein and floral display suggested pollen amino acid concentrations drove insect preference among plant species when floral display sizes were large. We show that floral resource quality is sensitive to agrochemical exposure and that flower-visiting insects are sensitive to variation in floral resource quality.

Pesticide mixtures detected in crop and non-target wild plant pollen and nectar.

Cultivation of mass flowering entomophilous crops benefits from the presence of managed and wild pollinators, who visit flowers to forage on pollen and nectar. However, management of these crops typically includes application of pesticides, the presence of which may pose a hazard for pollinators foraging in an agricultural environment. To determine the levels of potential exposure to pesticides, their presence and concentration in pollen and nectar need assessing, both within and beyond the target crop plants. We selected ten pesticide compounds and one metabolite and analysed their occurrence in a crop (Brassica napus) and a wild plant (Rubus fruticosus agg.), which was flowering in field edges. Nectar and pollen from both plants were collected from five spring and five winter sown B. napus fields in Ireland, and were tested for pesticide residues, using QuEChERS and Liquid Chromatography tandem mass spectrometry (LC-MS/MS). Pesticide residues were detected in plant pollen and nectar of both plants. Most detections were from fields with no recorded application of the respective compounds in that year, but higher concentrations were observed in recently treated fields. Overall, more residues were detected in B. napus pollen and nectar than in the wild plant, and B. napus pollen had the highest mean concentration of residues. All matrices were contaminated with at least three compounds, and the most frequently detected compounds were fungicides. The most common compound mixture was comprised of the fungicides azoxystrobin, boscalid, and the neonicotinoid insecticide clothianidin, which was not recently applied on the fields. Our results indicate that persistent compounds like the neonicotinoids, should be continuously monitored for their presence and fate in the field environment. The toxicological evaluation of the compound mixtures identified in the present study should be performed, to determine their impacts on foraging insects that may be exposed to them.

Plant protection product residues in plant pollen and nectar: A review of current knowledge.

Exposure to Plant Protection Products, PPPs, (fungicides, herbicides and insecticides) is a significant stressor for bees and other pollinators, and has recently been the focus of intensive debate and research. Specifically, exposure through contaminated pollen and nectar is considered pivotal, as it presents the highest risk of PPP exposure across all bee species. However, the actual risk that multiple PPP residues might pose to non-target species is difficult to assess due to the lack of clear evidence of their actual concentrations. To consolidate the existing knowledge of field-realistic residues detected in pollen and nectar directly collected from plants, we performed a systematic literature review of studies over the past 50 years (1968-2018). We found that pollen was the matrix most frequently evaluated and, of the compounds investigated, the majority were detected in pollen samples. Although the overall most studied category of PPPs were the neonicotinoid insecticides, the compounds with the highest median concentrations of residues in pollen were: the broad spectrum carbamate carbofuran (1400 ng/g), the fungicide and nematicide iprodione (524 ng/g), and the organophosphate insecticide dimethoate (500 ng/g). In nectar, the highest median concentration of PPP residues detected were dimethoate (1595 ng/g), chlorothalonil (76 ng/g), and the insecticide phorate (53.5 ng/g). Strong positive correlation was observed between neonicotinoid residues in pollen and nectar of cultivated plant species. The maximum concentrations of several compounds detected in nectar and pollen were estimated to exceed the LD50s for honey bees, bumble bees and four solitary bee species, by several orders of magnitude. However, there is a paucity of information for the biggest part of the world and there is an urgent need to expand the range of compounds evaluated in PPP studies.

Bees prefer foods containing neonicotinoid pesticides.

The impact of neonicotinoid insecticides on insect pollinators is highly controversial. Sublethal concentrations alter the behaviour of social bees and reduce survival of entire colonies. However, critics argue that the reported negative effects only arise from neonicotinoid concentrations that are greater than those found in the nectar and pollen of pesticide-treated plants. Furthermore, it has been suggested that bees could choose to forage on other available flowers and hence avoid or dilute exposure. Here, using a two-choice feeding assay, we show that the honeybee, Apis mellifera, and the buff-tailed bumblebee, Bombus terrestris, do not avoid nectar-relevant concentrations of three of the most commonly used neonicotinoids, imidacloprid (IMD), thiamethoxam (TMX), and clothianidin (CLO), in food. Moreover, bees of both species prefer to eat more of sucrose solutions laced with IMD or TMX than sucrose alone. Stimulation with IMD, TMX and CLO neither elicited spiking responses from gustatory neurons in the bees' mouthparts, nor inhibited the responses of sucrose-sensitive neurons. Our data indicate that bees cannot taste neonicotinoids and are not repelled by them. Instead, bees preferred solutions containing IMD or TMX, even though the consumption of these pesticides caused them to eat less food overall. This work shows that bees cannot control their exposure to neonicotinoids in food and implies that treating flowering crops with IMD and TMX presents a sizeable hazard to foraging bees.